Evidence for a Xer/dif system for chromosome resolution in archaea

PLoS Genetics

Volumn 6, Issue 10, 2010, Pages 1-11

  Cortez, Diego ^a,d   Quevillon Cheruel, Sophie ^b   Gribaldo, Simonetta ^a   Desnoues, Nicole ^a   Sezonov, Guennadi ^a,c   Forterre, Patrick ^a,b   Serre, Marie Claude ^b  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; RECOMBINASE; UNCLASSIFIED DRUG; XERA RECOMBINASE; ARCHAEAL DNA; ARCHAEAL PROTEIN; CIRCULAR DNA; DNA POLYMERASE; SITE SPECIFIC RECOMBINASE; SITE-SPECIFIC RECOMBINASE;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; CHROMOSOMAL LOCALIZATION; CHROMOSOME REPLICATION; COMPUTER MODEL; COMPUTER PREDICTION; CONTROLLED STUDY; GENETIC MODEL; GENETIC RECOMBINATION; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PYROCOCCUS ABYSSI; RECOMBINANT PLASMID; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ARCHAEBACTERIUM; BINDING SITE; CHROMOSOME; CLASSIFICATION; DNA REPLICATION; ENZYMOLOGY; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PLASMID; PROTEIN BINDING;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PYROCOCCUS ABYSSI; XERA;

AMINO ACID SEQUENCE; ARCHAEA; ARCHAEAL PROTEINS; BINDING SITES; CHROMOSOMES, ARCHAEAL; CLONING, MOLECULAR; DNA NUCLEOTIDYLTRANSFERASES; DNA REPLICATION; DNA, ARCHAEAL; DNA, CIRCULAR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; PROTEIN BINDING; PYROCOCCUS ABYSSI; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 78449246348     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001166     Document Type: Article

References (55)

1. Blakely G, May G, McCulloch R, Arciszewska LK, Burke M, et al. (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75: 351-361.
2. Blakely G, Colloms S, May G, Burke M, Sherratt D (1991) Escherichia coli XerC recombinase is required for chromosomal segregation at cell division. New Biol 3: 789-798.
3. Clerget M (1991) Site-specific recombination promoted by a short DNA segment of plasmid R1 and by a homologous segment in the terminus region of the Escherichia coli chromosome. New Biol 3: 780-788.
4. Kuempel PL, Henson JM, Dircks L, Tecklenburg M, Lim DF (1991) dif, a recAindependent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol 3: 799-811.
5. Carnoy C, Roten CA (2009) The dif/Xer recombination systems in proteobacteria. PLoS One 4: e6531. doi:10.1371/journal.pone.0006531.
6. Jensen RB (2006) Analysis of the terminus region of the Caulobacter crescentus chromosome and identification of the dif site. J Bacteriol 188: 6016-6019.
7. Neilson L, Blakely G, Sherratt DJ (1999) Site-specific recombination at dif by Haemophilus influenzae XerC. Mol Microbiol 31: 915-926.
8. Sciochetti SA, Piggot PJ, Blakely GW (2001) Identification and characterization of the dif Site from Bacillus subtilis. J Bacteriol 183: 1058-1068.
9. Val ME, Kennedy SP, El Karoui M, Bonne L, Chevalier F, et al. (2008) FtsKdependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet 4: e1000201. doi:10.1371/journal.pgen.1000201.
10. Yen MR, Lin NT, Hung CH, Choy KT, Weng SF, et al. (2002) oriC region and replication termination site, dif, of the Xanthomonas campestris pv. campestris 17 chromosome. Appl Environ Microbiol 68: 2924-2933.
11. Blakely GW, Sherratt DJ (1994) Interactions of the site-specific recombinases XerC and XerD with the recombination site dif. Nucleic Acids Res 22: 5613-5620.
12. Aussel L, Barre FX, Aroyo M, Stasiak A, Stasiak AZ, et al. (2002) FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108: 195-205.
13. Barre FX, Aroyo M, Colloms SD, Helfrich A, Cornet F, et al. (2000) FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev 14: 2976-2988.
14. Ip SC, Bregu M, Barre FX, Sherratt DJ (2003) Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J 22: 6399-6407.
15. Steiner W, Liu G, Donachie WD, Kuempel P (1999) The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol Microbiol 31: 579-583.
16. Bigot S, Saleh OA, Lesterlin C, Pages C, El Karoui M, et al. (2005) KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 24: 3770-3780.
17. Corre J, Louarn JM (2002) Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli. J Bacteriol 184: 3801-3807.
18. Levy O, Ptacin JL, Pease PJ, Gore J, Eisen MB, et al. (2005) Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci U S A 102: 17618-17623.
19. Pease PJ, Levy O, Cost GJ, Gore J, Ptacin JL, et al. (2005) Sequence-directed DNA translocation by purified FtsK. Science 307: 586-590.
20. Sivanathan V, Allen MD, de Bekker C, Baker R, Arciszewska LK, et al. (2006) The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol 13: 965-972.
21. Yates J, Zhekov I, Baker R, Eklund B, Sherratt DJ, et al. (2006) Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol Microbiol 59: 1754-1766.
22. Le Bourgeois P, Bugarel M, Campo N, Daveran-Mingot ML, Labonte J, et al. (2007) The unconventional Xer recombination machinery of Streptococci/ Lactococci. PLoS Genet 3: e117. doi:10.1371/journal.pgen.0030117.
23. Haldenby S, White MF, Allers T (2009) RecA family proteins in archaea: RadA and its cousins. Biochem Soc Trans 37: 102-107.
24. Serre MC, Duguet M (2003) Enzymes that cleave and religate DNA at high temperature: the same story with different actors. Prog Nucleic Acid Res Mol Biol 74: 37-81.
25. Kanehisa M, Goto S, Kawashima S, Nakaya A (2002) The KEGG databases at GenomeNet. Nucleic Acids Res 30: 42-46.
26. Sherratt DJ, Wigley DB (1998) Conserved themes but novel activities in recombinases and topoisomerases. Cell 93: 149-152.
27. Cao Y, Hallet B, Sherratt DJ, Hayes F (1997) Structure-function correlations in the XerD site-specific recombinase revealed by pentapeptide scanning mutagenesis. J Mol Biol 274: 39-53.
28. Spiers AJ, Sherratt DJ (1997) Relating primary structure to function in the Escherichia coli XerD site-specific recombinase. Mol Microbiol 24: 1071-1082.
29. Subramanya HS, Arciszewska LK, Baker RA, Bird LE, Sherratt DJ, et al. (1997) Crystal structure of the site-specific recombinase, XerD. EMBO J 16: 5178-5187.
30. Lillestol RK, Redder P, Garrett RA, Brugger K (2006) A putative viral defence mechanism in archaeal cells. Archaea 2: 59-72.
31. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1: 7.
32. Zivanovic Y, Lopez P, Philippe H, Forterre P (2002) Pyrococcus genome comparison evidences chromosome shuffling-driven evolution. Nucleic Acids Res 30: 1902-1910.
33. Myllykallio H, Lopez P, Lopez-Garcia P, Heilig R, Saurin W, et al. (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288: 2212-2215.
34. Lopez P, Philippe H, Myllykallio H, Forterre P (1999) Identification of putative chromosomal origins of replication in Archaea. Mol Microbiol 32: 883-886.
35. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
36. Lundgren M, Andersson A, Chen L, Nilsson P, Bernander R (2004) Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc Natl Acad Sci U S A 101: 7046-7051.
37. Robinson NP, Dionne I, Lundgren M, Marsh VL, Bernander R, et al. (2004) Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell 116: 25-38.
38. Hoebeke M, Schbath S (2006) R'MES: Finding Exceptional Motifs, version 3. User guide http://genome.jouy.inra.fr/ssb/rmes.
39. Serre MC, Letzelter C, Garel JR, Duguet M (2002) Cleavage properties of an archaeal site-specific recombinase, the SSV1 integrase. J Biol Chem 277: 16758-16767.
40. Hayes F, Sherratt DJ (1997) Recombinase binding specificity at the chromosome dimer resolution site dif of Escherichia coli. J Mol Biol 266: 525-537.
41. Cornet F, Hallet B, Sherratt DJ (1997) Xer recombination in Escherichia coli. Sitespecific DNA topoisomerase activity of the XerC and XerD recombinases. J Biol Chem 272: 21927-21931.
42. Constantinesco F, Forterre P, Koonin EV, Aravind L, Elie C (2004) A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res 32: 1439-1447.
43. Quaiser A, Constantinesco F, White MF, Forterre P, Elie C (2008) The Mre11 protein interacts with both Rad50 and the HerA bipolar helicase and is recruited to DNA following gamma irradiation in the archaeon Sulfolobus acidocaldarius. BMC Mol Biol 9: 25.
44. Zhang S, Wei T, Hou G, Zhang C, Liang P, et al. (2008) Archaeal DNA helicase HerA interacts with Mre11 homologue and unwinds blunt-ended doublestranded DNA and recombination intermediates. DNA Repair (Amst) 7: 380-391.
45. Iyer LM, Makarova KS, Koonin EV, Aravind L (2004) Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32: 5260-5279.
46. Colloms SD, Alen C, Sherratt DJ (1998) The ArcA/ArcB two-component regulatory system of Escherichia coli is essential for Xer site-specific recombination at psi. Mol Microbiol 28: 521-530.
47. Cornet F, Mortier I, Patte J, Louarn JM (1994) Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol 176: 3188-3195.
48. Stirling CJ, Colloms SD, Collins JF, Szatmari G, Sherratt DJ (1989) xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase. EMBO J 8: 1623-1627.
49. Stirling CJ, Szatmari G, Stewart G, Smith MC, Sherratt DJ (1988) The arginine repressor is essential for plasmid-stabilizing site-specific recombination at the ColE1 cer locus. EMBO J 7: 4389-4395.
50. Lundgren M, Bernander R (2007) Genome-wide transcription map of an archaeal cell cycle. Proc Natl Acad Sci U S A 104: 2939-2944.
51. Forterre P (1999) Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 33: 457-465.
52. Forterre P (2002) The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol 5: 525-532.
53. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
54. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
55. Kim J, Zwieb C, Wu C, Adhya S (1989) Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector. Gene 85: 15-23.